Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield

Nyyssönen, Mari; Hultman, Jenni; Ahonen, Lasse; Kukkonen, Ilmo; Paulín, Lars; Laine, Pia; Itävaara, Merja; Auvinen, Petri

doi:10.1038/ismej.2013.125

Cited by 111 publications

(157 citation statements)

References 39 publications

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“…(mg/L) ME-7 The bacterial clone analysis results suggested that shared OTUs between samples were less and 168 in 201 OTUs were unique to each sample, showing same result as previous studies [4,16]. Meanwhile, some sequences, closely related to taxa involved in various metabolic processes, were simultaneously found in a single sample (Fig.…”

Section: Correlation Between Bacterial Distribution and Hydrochemicalsupporting

confidence: 81%

“…Microorganisms in the aquifer have to develop adaptation mechanisms for survival under oligotrophic conditions in a subsurface environment. Thus, geochemical conditions and particularly availability of electron donors and acceptors are major drivers of microbial composition and diversity in groundwater and geological substratum [3,4]. Additionally, the groundwater system displays pronounced spatial heterogeneity, as a result of the stratified nature of many subsurface deposits.…”

Section: Introductionmentioning

confidence: 99%

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Spatial Distribution of Microbial Communities in the Alluvial Aquifer along the Oyodo River, Miyakonojo Basin, Japan

Zeng

Hosono

Matsunaga

et al. 2017

J. of Wat. & Envir. Tech.

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The hydrogeological properties of groundwater and behavior of nitrate attenuation in the nitratepolluted alluvial aquifer, Miyakonojo Basin have been investigated in previous studies, but little knowledge is known about the spatially microbial communities especially associated with nitrate depletion. The objectives of the present study are to reveal the profile of microbial communities in the alluvial aquifer, Miyakonojo Basin, and the association with environmental variations based on cloning-library approach together with hydrogeochemical variables. The results showed that high bacterial diversity was characteristic of a large number of operational taxonomic units unique to the samples. The presence of some human-/livestock related bacteria was consistent with the distribution of high nitrate concentrations, which indicated an influence of hydrogeochemical variables on microbial composition. Methane-producing archaea and ammonia-oxidizing archaea were primarily found in the anoxic and oxic environments, respectively, reflected by the distribution of welded tuff. Additionally, heterotrophic and mixo-/autotrophic denitrifiers were ubiquitously distributed, but denitrification process only occurred under the anoxic environment. Microorganisms involved in the various metabolic processes were found to coexist in the same samples. Together, this study suggested that the description of microbial communities profile and associated putative metabolic processes could reflect the hydrogeochemical conditions of the alluvial aquifer, Miyakonojo Basin.

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Section: Correlation Between Bacterial Distribution and Hydrochemicalsupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Spatial Distribution of Microbial Communities in the Alluvial Aquifer along the Oyodo River, Miyakonojo Basin, Japan

Zeng

Hosono

Matsunaga

et al. 2017

J. of Wat. & Envir. Tech.

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“…Of the viral contigs, 86% belonged to members of the Caudovirales, tailed dsDNA viruses, with Myoviridae (44%) and Siphoviridae (26%) families predominating. Previously, only viral reads and prophage genome fragments have been reported 10,26,27 . We mined our microbial genomes for the presence of CRISPRCas systems (clustered regularly interspaced short palindromic repeat-CRISPR associated), which act as an acquired immunity to viruses 28 (Supplementary Table 8).…”

Section: Active Viral Predation In the Deep Subsurfacementioning

confidence: 99%

Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales

et al. 2016

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Hydraulic fracturing is the industry standard for extracting hydrocarbons from shale formations. Attention has been paid to the economic benefits and environmental impacts of this process, yet the biogeochemical changes induced in the deep subsurface are poorly understood. Recent single-gene investigations revealed that halotolerant microbial communities were enriched after hydraulic fracturing. Here, the reconstruction of 31 unique genomes coupled to metabolite data from the Marcellus and Utica shales revealed that many of the persisting organisms play roles in methylamine cycling, ultimately supporting methanogenesis in the deep biosphere. Fermentation of injected chemical additives also sustains long-term microbial persistence, while thiosulfate reduction could produce sulfide, contributing to reservoir souring and infrastructure corrosion. Extensive links between viruses and microbial hosts demonstrate active viral predation, which may contribute to the release of labile cellular constituents into the extracellular environment. Our analyses show that hydraulic fracturing provides the organismal and chemical inputs for colonization and persistence in the deep terrestrial subsurface. S hale gas accounts for one-third of natural gas energy resources worldwide. It has been estimated that shale gas will provide half of the natural gas in the USA, annually, by 2040, with the Marcellus shale in the Appalachian Basin projected to produce three times more than any other formation 1 . Recovery of these hydrocarbons is dependent on hydraulic fracturing technologies, where the high-pressure injection of water and chemical additives generates extensive fractures in the shale matrix. Hydrocarbons trapped in tiny pore spaces are subsequently released and collected at the wellpad surface, together with a portion of the injected fluids that have reacted with the shale formation. The mixture of injected fluids and hydrocarbons collected is referred to as 'produced fluids'.Microbial metabolism and growth in hydrocarbon reservoirs has both positive and negative impacts on energy recovery. Whereas stimulation of methanogens in coal beds enhances energy recovery 2 , bacterial hydrogen sulfide production ('reservoir souring') decreases profits and contributes to corrosion and the risk of environmental contamination 3 . Additionally, biomass accumulation within newly generated fractures may reduce their permeability, decreasing natural gas recovery. Despite these potential microbial impacts, little is known about the function and activity of microorganisms in hydraulically fractured shale.Initial work by our group and others 4-9 used single marker gene analyses to identify microorganisms from several geographically distinct shale formations. These analyses showed similar halotolerant taxa in produced fluids several months after hydraulic fracturing. To assign functional roles to these organisms, we conducted metagenomic and metabolite analyses on input and produced fluids up to a year after hydraulic fracturing (HF) from two Appala...

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“…In oligotrophic systems, subsurface lithoautotrophic microbial ecosystems (SLiMEs) (1) that are fueled by H 2 support the occurrence of autotrophic methanogens, acetogens, and sulfate reducers (2)(3)(4)(5). These environments can host highly diverse communities, consisting mostly of prokaryotes, but also multicellular microeukaryotes and viral particles (6)(7)(8)(9)(10)(11)(12)(13). Due to the limitation of available nutrients and energy substrates in the oligotrophic subsurface, it is reasonable to hypothesize that subsurface inhabitants with diverse functional traits cooperate syntrophically to maximize energy yield…”

mentioning

confidence: 99%

An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers

Lau

Kieft

Kuloyo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

177

199

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Subsurface lithoautotrophic microbial ecosystems (SLiMEs) under oligotrophic conditions are typically supported by H 2 . Methanogens and sulfate reducers, and the respective energy processes, are thought to be the dominant players and have been the research foci. Recent investigations showed that, in some deep, fluid-filled fractures in the Witwatersrand Basin, South Africa, methanogens contribute <5% of the total DNA and appear to produce sufficient CH 4 to support the rest of the diverse community. This paradoxical situation reflects our lack of knowledge about the in situ metabolic diversity and the overall ecological trophic structure of SLiMEs. Here, we show the active metabolic processes and interactions in one of these communities by combining metatranscriptomic assemblies, metaproteomic and stable isotopic data, and thermodynamic modeling. Dominating the active community are four autotrophic β-proteobacterial genera that are capable of oxidizing sulfur by denitrification, a process that was previously unnoticed in the deep subsurface. They co-occur with sulfate reducers, anaerobic methane oxidizers, and methanogens, which each comprise <5% of the total community. Syntrophic interactions between these microbial groups remove thermodynamic bottlenecks and enable diverse metabolic reactions to occur under the oligotrophic conditions that dominate in the subsurface. The dominance of sulfur oxidizers is explained by the availability of electron donors and acceptors to these microorganisms and the ability of sulfur-oxidizing denitrifiers to gain energy through concomitant S and H 2 oxidation. We demonstrate that SLiMEs support taxonomically and metabolically diverse microorganisms, which, through developing syntrophic partnerships, overcome thermodynamic barriers imposed by the environmental conditions in the deep subsurface.active subsurface environment | metabolic interactions | sulfur-driven autotrophic denitrifiers | syntrophy | inverted biomass pyramid M icroorganisms living in deep-subsurface ecosystems acquire energy through chemosynthesis and carbon from organic or inorganic sources. Whereas heterotrophs use dissolved organic carbon (DOC) transported from the surface and/or produced in situ, detrital organic deposits buried along with the sediments, and hydrocarbons migrating into petroleum reservoirs, chemolithoautotrophs fix dissolved inorganic carbon (DIC). In oligotrophic systems, subsurface lithoautotrophic microbial ecosystems (SLiMEs) (1) that are fueled by H 2 support the occurrence of autotrophic methanogens, acetogens, and sulfate reducers (2-5). These environments can host highly diverse communities, consisting mostly of prokaryotes, but also multicellular microeukaryotes and viral particles (6-13). Due to the limitation of available nutrients and energy substrates in the oligotrophic subsurface, it is reasonable to hypothesize that subsurface inhabitants with diverse functional traits cooperate syntrophically to maximize energy yield SignificanceMicroorganisms are known to live in the deep ...

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Taxonomically and functionally diverse microbial communities in deep crystalline rocks of the Fennoscandian shield

Cited by 111 publications

References 39 publications

Spatial Distribution of Microbial Communities in the Alluvial Aquifer along the Oyodo River, Miyakonojo Basin, Japan

Spatial Distribution of Microbial Communities in the Alluvial Aquifer along the Oyodo River, Miyakonojo Basin, Japan

Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales

An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers

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